Engraftment of a Clonal Bone Marrow Stromal Cell Line in Vivo Stimulates Hematopoietic Recovery from Total Body Irradiation

Overview

Journal Proc Natl Acad Sci U S A

Specialty Science

Date 1987 Nov 1

PMID 2890167

Citations 24

Authors

P Anklesaria

K Kase

J Glowacki

C A Holland

M A Sakakeeny

J A Wright

T J Fitzgerald

C Y Lee

J S Greenberger

Affiliations

Soon will be listed here.

Abstract

Whether bone marrow stromal cells of donors contribute physiologically to hematopoietic stem cell reconstitution after marrow transplantation is unknown. To determine the transplantability of nonhematopoietic marrow stromal cells, stable clonal stromal cell line (GB1/6) expressing the a isoenzyme of glucose-6-phosphate isomerase (Glu6PI-a, D-glucose-6-phosphate ketol-isomerase; EC 5.3.1.9) was derived from murine long-term bone marrow cultures and made resistant to neomycin analogue G418 by retroviral gene transfer. GB1/6 cells were fibronectin+, laminin+, and collagen-type IV+ and collagen type I-; these GB1/6 cells supported in vitro growth of hematopoietic stem cells forming colony-forming units of spleen cells (CFU-S) and of granulocytes, erythrocytes, and macrophage/megakarocytes (CFU-GEMM) in the absence of detectable growth factors interleukin 3 (multi-colony-stimulating factor), granulocyte/macrophage colony-stimulating factor, granulocyte-stimulating factor, or their poly(A)+ mRNAs. The GB1/6 cells produced macrophage colony-stimulating factor constitutively. Recipient C57BL/6J (glucose-6-phosphate isomerase b) mice that received 3-Gy total-body irradiation and 13 Gy to the right hind limb were injected i.v. with GB1/6 cells. Engrafted mice demonstrated donor-originating Glu6PI-a+ stromal cells in marrow sinuses in situ 2 mo after transplantation and a significantly enhanced hematopoietic recovery compared with control irradiated nontransplanted mice. Continuous (over numerous passages) marrow cultures derived from transplanted mice demonstrated G418-resistant, Glu6PI-a+ stromal colony-forming cells and greater cumulative production of multipotential stem cells of recipient origin compared with cultures established from irradiated, nontransplanted control mice. These data are evidence for physiological function in vivo of a transplanted bone marrow stromal cell line.

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References

Chamberlin W, Barone J, Kedo A, Fried W . Lack of recovery of murine hematopoietic stromal cells after irradiation-induced damage. Blood. 1974; 44(3):385-92. View

Greenberger J . Sensitivity of corticosteroid-dependent insulin-resistant lipogenesis in marrow preadipocytes of obese-diabetic (db/db) mice. Nature. 1978; 275(5682):752-4. DOI: 10.1038/275752a0. View

Werts E, Gibson D, Knapp S, DEGOWIN R . Stromal cell migration precedes hemopoietic repopulation of the bone marrow after irradiation. Radiat Res. 1980; 81(1):20-30. View

Charles D, Lee C . Biochemical characterization of phosphoglucose isomerase and genetic variants from mouse and Drosophila melanogaster. Mol Cell Biochem. 1980; 29(1):11-21. DOI: 10.1007/BF00230952. View

Golde D, Hocking W, Quan S, Sparkes R, Gale R . Origin of human bone marrow fibroblasts. Br J Haematol. 1980; 44(2):183-7. DOI: 10.1111/j.1365-2141.1980.tb01200.x. View

BRECHER G, Tjio J, Haley J, Narla J, Beal S . Transplantation of murine bone marrow without prior host irradiation. Blood Cells. 1979; 5(2):237-46. View

Humphries R, Eaves A, Eaves C . Self-renewal of hemopoietic stem cells during mixed colony formation in vitro. Proc Natl Acad Sci U S A. 1981; 78(6):3629-33. PMC: 319624. DOI: 10.1073/pnas.78.6.3629. View

Magli M, Iscove N, ODARTCHENKO N . Transient nature of early haematopoietic spleen colonies. Nature. 1982; 295(5849):527-9. DOI: 10.1038/295527a0. View

Keating A, Singer J, Killen P, Striker G, Salo A, Sanders J . Donor origin of the in vitro haematopoietic microenvironment after marrow transplantation in man. Nature. 1982; 298(5871):280-3. DOI: 10.1038/298280a0. View

10.

Greenberger J, Eckner R, Otten J, Tennant R . In vitro quantitation of lethal and physiologic effects of total body irradiation on stromal and hematopoietic stem cells in continuous bone marrow cultures from Rf mice. Int J Radiat Oncol Biol Phys. 1982; 8(7):1155-65. DOI: 10.1016/0360-3016(82)90063-3. View

11.

Piersma A, Ploemacher R, Brockbank K . Transplantation of bone marrow fibroblastoid stromal cells in mice via the intravenous route. Br J Haematol. 1983; 54(2):285-90. DOI: 10.1111/j.1365-2141.1983.tb02097.x. View

12.

Fung M, Hapel A, Ymer S, Cohen D, Johnson R, Campbell H . Molecular cloning of cDNA for murine interleukin-3. Nature. 1984; 307(5948):233-7. DOI: 10.1038/307233a0. View

13.

Juneja H, GARDNER F, Minguell J, Helmer 3rd R . Abnormal marrow fibroblasts in aplastic anemia. Exp Hematol. 1984; 12(4):221-30. View

14.

Marshall M, Nisbet N, Evans S . Donor origin of the in vitro hematopoietic microenvironment after marrow transplantation in mice. Experientia. 1984; 40(4):385-6. DOI: 10.1007/BF01952566. View

15.

Gough N, Gough J, Metcalf D, Kelso A, Grail D, Nicola N . Molecular cloning of cDNA encoding a murine haematopoietic growth regulator, granulocyte-macrophage colony stimulating factor. Nature. 1984; 309(5971):763-7. DOI: 10.1038/309763a0. View

16.

Champlin R, Feig S, Gale R . Case problems in bone marrow transplantation. I. Graft failure in aplastic anemia: its biology and treatment. Exp Hematol. 1984; 12(9):728-33. View

17.

Zipori D, Duksin D, Tamir M, Argaman A, Toledo J, Malik Z . Cultured mouse marrow stromal cell lines. II. Distinct subtypes differing in morphology, collagen types, myelopoietic factors, and leukemic cell growth modulating activities. J Cell Physiol. 1985; 122(1):81-90. DOI: 10.1002/jcp.1041220113. View

18.

Auron P, Webb A, Rosenwasser L, Mucci S, Rich A, Wolff S . Nucleotide sequence of human monocyte interleukin 1 precursor cDNA. Proc Natl Acad Sci U S A. 1984; 81(24):7907-11. PMC: 392262. DOI: 10.1073/pnas.81.24.7907. View

19.

Ramsay N, LeBien T, Nesbit M, McGlave P, Weisdorf D, Kenyon P . Autologous bone marrow transplantation for patients with acute lymphoblastic leukemia in second or subsequent remission: results of bone marrow treated with monoclonal antibodies BA-1, BA-2, and BA-3 plus complement. Blood. 1985; 66(3):508-13. View

20.

Takahashi M, Keating A, Singer J . A functional defect in irradiated adherent layers from chronic myelogenous leukemia long-term marrow cultures. Exp Hematol. 1985; 13(9):926-31. View